The PII superfamily consists of widespread signal transduction proteins found in all domains of life. The most conserved PII-interactor across oxygenic phototrophs from cyanobacteria to Archaeplastida is the key enzyme of the ornithine/arginine synthesis pathway, N-acetyl-L-glutamate kinase (NAGK). T-loops represent the major PII-receptor binding element and are involved in the interaction with NAGK. Within the class Mamiellophyceae, only the genus Micromonas contains species with the PII protein. Bioinformatic analysis revealed that the PII protein of Micromonas pusilla (MpPII) has an unusually prolonged T-loop. Here, we performed the coupled enzyme assay and showed that MpPII has no remarkable influence on NAGK activity. An engineered variant of MpPII with deletion of four additional amino acids (AATD) in the T-loop restored the ability of this protein to relieve NAGK from feedback inhibition by arginine in a glutamine-dependent manner. The findings are discussed in the context of unusual plasticity of the PII protein family during the evolution of Archaeplastida.